diet and functional morphology of the mandible of two ... and functional.pdf · morphology, the...

DIET AND FUNCTIONAL MORPHOLOGY OF THE MANDIBLEOF TWO PLANKTONIC AMPHIPODS FROM THE STRAIT OF GEORGIA

BRITISH COLUMBIA PARATHEMISTOPACIFICA (STEBBING 1888)AND CYPHOCARIS CHALLENGERI (STEBBING 1888)

BY

MARTHA J HARO-GARAY1

University of British Columbia Oceanography Group Biological Sciences West WingRoom 1461 6270 University Boulevard Vancouver British Columbia V6T 1Z4 Canada

ABSTRACT

In amphipods morphological adaptations for feeding provide taxonomic evidence that helps todifferentiate them into species Intuitively this indicates that the morphology of feeding structuresmay be related to the type of food the amphipods consume This hypothesis was examined usingzooplankton collections from three locations from the Strait of Georgia British Columbia theFraser River plume the estuarine plume and the Strait The study investigated the mandiblemorphology the stomach contents and the potential food for the amphipods Parathemisto pacicaand Cyphocaris challengeri

Mandible morphology obtained with SEM photography and morphometric analyses was usedto infer feeding habits The mandible of P pacica has a wide molar indicative of microphagoushabits and a cutting incisor related to carnivorous habits while in C challengeri the strong molarand sharp incisor in the mandible indicate carnivorous habits Stomach contents indicated that bothParathemisto pacica and Cyphocaris challengeri preyed most frequently on copepods amphipodscladocerans and ostracodes The amphipods appeared to select female copepods perhaps eitherbecause females can have a higher nutritious value when bearing eggs or because they are moreabundant than male copepodsThe difference in the diet between the two specieswas that amphipodswere more abundant in stomachs of C challengeri and copepods were more numerous in thestomachs of P pacica The presence of small copepod species in the diet of amphipods suggestsamphipods are an important link between nanoplankton the food of copepods and the sh thatconsume amphipods (eg salmonids and clupeids)

ZUSAMMENFASSUNG

Anpassungen im Zusammenhang mit der Nahrungsaufnahme sind bei Amphipoden eine Hilfebei der Artabgrenzung Rein intuitiv zeigt dies dass eine Beziehung bestehen kann zwischen demBau der Nahrungsaufnahmeorganeund der Art der Nahrung die von den Amphipoden konsumiert

1 e-mail harointerchangeubcca

copy Koninklijke Brill NV Leiden 2004 Crustaceana 76 (11) 1291-1312Also available online wwwbrillnl

1292 MARTHA J HARO-GARAY

wird Zur Pruumlfung dieser Hypothese wurden Zooplanktonproben von drei Standorten der Georgia-Straszlige Britisch-Columbia untersucht aus der Fahne des Fraser Flusses der Muumlndungsfahne undder Georgia-Straszlige Untersucht wurden der Bau der Mandibel der Mageninhalt und die potentielleNahrung der Amphipoden Parathemisto pacica und Cyphocaris challengeri

Rasterelektronenmikroskopische Aufnahmen der Mandibel und morphometrischeAnalysen wur-den benutzt um auf Nahrungsgewohnheitenruumlckzuschlieszligen Die Mandibel von P pacica hat einebreite pars molaris die auf Mikrophagiehindeutet und eine Schneidekantedie eher eischfressendeGewohnheiten nahelegt C challengeri dagegen scheint mit seiner kraumlftigen pars molaris und schar-fen Schneidekante der Mandibel ein richtiger Fleischfresser zu sein Die Mageninhaltsuntersuchun-gen zeigten dass sowohl Parathemistopacica als auch Cyphocaris challengerihauptsaumlchlich Cope-poden Amphipoden Cladocerenund Ostracoden erbeutenBeide scheinen Copepoden-Weibchenzubevorzugen entweder wegen ihres houmlheren Naumlhrwerts wenn sie Eier tragen oder weil sie die Maumln-nchen an Zahl uumlbertreffen Der Unterschied in der Nahrung beider Arten bestand darin dass derMagen von C challengeri mehr Amphipoden und der von P pacica mehr Copepoden enthielt DieTatsache dass kleine Copepoden-Artenzur Nahrung von Amphipoden gehoumlren legt nahe dass dieseein wichtiges Bindeglied zwischen dem Nanoplankton von dem sich die Copepoden ernaumlhren undFischen sind (zB Salmoniden und Clupeiden) die Amphipoden verzehren

INTRODUCTION

Amphipods are abundant in cold environments (Bowman amp Gruner 1973)particularly in highly productive estuarine areas (Nair et al 1973) as the Straitof Georgia British Columbia (St John et al 1992) They can be an important partof the diet of whales (Nemoto 1970) and sh (Birtwell et al 1984 St John et al1992) including salmon (Beacham 1986 Brodeur 1990) and keen zooplanktonpredators as well (Sheader amp Evans 1975) Knowledge of the feeding habits ofamphipods can provide a better understanding of the role they play in the trophicecology of the Strait of Georgia estuary

The study reported here was based on the hypothesis that because of environ-mental adaptations there is a strong relationship between morphology and ecolog-ical characteristics (Reilly amp Wainwright 1994) The morphology of the mandibleand of the rest of the feeding appendages is widely used for taxonomic classi -cation of amphipods (Barnard 1958) and the variation across species has provedquite useful in phylogenetic research (Watling 1993 Bous eld 1995) Yet only ahandful of studies has focused on the connection between morphology of oral ap-pendages and ecology (eg Sainte-Marie 1984 Moore amp Rainbow 1989 Cole-man 1991a b Steele amp Steele 1993)

The premise was that the morphology of the mandible and feeding habits areclosely related Testing this hypothesis involved investigating the mandible mor-phology and stomach contents of the amphipods Cyphocaris challengeri Stebbing1888 and Parathemisto paci ca Stebbing 1888 species abundant in plankton col-lections from the Strait of Georgia The study devoted particular attention to themandible morphology because among the mouthparts of amphipods the mandible

MANDIBLE MORPHOLOGY PLANKTONIC AMPHIPODS 1293

Fig 1 Schematic representationof an amphipod A body parts B head showing mouthparts (MX1maxilla 1 MX2 maxilla 2 MXP maxilliped) C mandible [A Redrawn from Bowman amp Gruner

1970 C redrawn from Schmitz 1992]

has the greatest interspeci c variation in shape which can be related to feedinghabits (Watling 1993)

The mandible of amphipods is located ventrally on the head in the bucal mass( g 1A) The bucal mass contains one pair of mandibles two pairs of biramousmaxillae and one pair of basally fused maxillipeds ( g 1B) The mandiblesthe maxillae and the maxillipeds each bear a palp (Bous eld 1973) except in


hyperiids which lack the palp in the maxilliped (Bowman amp Gruner 1973) Thebasic mandible of amphipods ( g 1C) consists of a compact coxa or mandiblebody bearing a toothed incisor a lacinia mobilis a row of setae leading dorsally toa molar designed for crushing and a 3-article palp (Manton 1977 Watling 1993)Parts most susceptible to change are the incisor and the molar The changes caninclude a reduction of the incisor loss of the seta row reduction or loss of themolar or all of these (Watling 1993)

The objective of this study was to investigate the mandible morphology ofP paci ca and C challengeri in order to make inferences on what type of foodthey may be able to consume Then their stomach contents were analysed toverify what they were actually eating The mandibles of P paci ca and C chal-lengeri were previously described in drawings by Bowman (1960) and Barnard(1958) respectively However such descriptions do not include information onthe functional morphology or the morphometrical changes the mandible un-dergoes during growth This information was considered fundamental to showwhat type of food the mandible would enable these animals to eat and whethermandible shape changed during growth Also stomach contents of both amphi-pod species were identi ed to investigate what the animals were actually eat-ing

MATERIALS AND METHODS

Amphipods were obtained from zooplankton samples collected in the Straitof Georgia British Columbia ( g 2) Samples were collected during 1990 and1991 in oblique hauls from 0-15 25 m depth with bongo nets of 296 sup1m and of300 sup1m mesh size (Clifford et al 1990 1991a b 1992 Harrison et al 1991)From these samples 32 Parathemisto paci ca and 38 Cyphocaris challengeriindividuals ( gs 3A B) were selected covering a size range from 2 to 16 mm Themandibles were dissected under a stereoscopic microscope and then immersed ina drop of corn syrup mixed with formalin (Pennak 1978) Mandible dimensionswere measured using an inverted microscope and a camera lucida The descriptionof cuticular extensions of the mandible such as spines and setae follows theterminology proposed by Watling (1989)

For Parathemisto paci ca the measurements taken to examine the mandiblemorphometry were length and height of the molar height and length of thecutting area of the incisor and number of teeth in the incisor For Cyphocarischallengeri the length and height of the molar the incisor height length of theincisor cutting area and length of the incisor base were taken In order to identifychanges in the mandible structure during growth all dimensions were regressed


Fig 2 Area of study the central Strait of Georgia R E S and DFO1 are the sampling stations inthis study R riverine plume E estuarine plume and S Strait

Fig 3 Amphipod species studiedA CyphocarischallengeriStebbing 1888 (adult approx 12 mm)B Parathemisto pacica Stebbing 1888 (adult approx 10 mm)

against body size Selected images of the mandibles were obtained by scanningelectron microscopy Preparation for scanning microscopy consisted of a series ofalcohol for dehydration critical point drying with CO2 and gold coating Electronmicroscopy was performed in the UBC Botany-Zoology Electron Microscopylaboratory with a conventional scanning electron microscope Zeiss EM 10c SEM

Stomach contents were emptied onto glass slides and examined under an in-verted microscope These contents were separated into pieces and the appearanceof each particle was recorded with as much detail as possible (eg round smallparticles spines cuticle pieces brown material etc) Food items found intact weremeasured and identi ed to the nearest taxonomic level according to criteria of se-lected literature The size of complete prey items was plotted against the size ofthe animal in which they were found


Fig 4 Scanning electron microscope image of Parathemisto pacica Stebbing 1888 mandibles

RESULTS

The mandible of Parathemisto paci ca

The mandibles are elongated have a thin integument insert laterally on thehead and meet frontally under the labrum The mandibular palps are directedfrontally on both sides of the labrum ( g 4) The labrum has a medioapicalnotch that covers the dorsal areas of the mandibles and partially overlaps themThe labium is bilobate each lobe is oval and wide ( g 4) The mandibles tbetween the labrum and the labium ( g 4) and surround the mouth The incisorsare wide and toothed and laterally anked on the external edge with a brush-looking set of long setae ( g 5) The teeth are sclerotized Only the left mandiblehas a lacinia mobilis which is about 30 smaller than the incisor and is similarlytoothed The left mandible embraces the right one between the incisor and thelacinia mobilis when closed The distal tooth on the left mandible ts betweenthe two distal teeth of the right mandible The molar arises from the frontal partof the mandible It is broad and round in small specimens and elongated andlanceolated in large specimens Its surface is covered with rows of lamellae withblunted sclerotized ridges ( g 6) The molar has a fringe structure with longersetae on the internal margin than those on the external margin Between the molarand the incisor process a small group of sharp setae protrudes forming the setarow ( gs 5-6)


Fig 5 Schematic representation of Parathemisto pacica Stebbing 1888 left mandible showing theincisor molar seta row and a detail of a seta

Fig 6 Scanning electronmicroscope image of Parathemisto pacica Stebbing 1888 mandible Notethe lamelliform rows with blunt cusps on the molar


Fig 7 Scanning electron microscope image of Parathemisto pacica Stebbing 1888 mouthpartsshowing the mandible and the mandible palp

Function of the mandible of Parathemisto paci ca

The frontal disposition of the incisors and their toothed cutting edges indicatethey work as a pair of trimming scissors Food may cling on the setae ankingthe external edges of the incisors during the cutting action and is pushed furtherinside mechanically with the next bite The medioapical notch of the labrum allowsthe use of the anterior incisor regions to produce a wide bite in which the rightmandible crosses between the incisor and the lacinia mobilis of the left mandiblein a cutting fashion The insertion of the distal tooth of the left incisor betweenthe pair of distal teeth of the right one suggests that when the mandibles closethe incisors come together in a clasping action for trimming and cutting The rowof setae adjacent to the incisor grasps and directs the food towards the molarsWhile the incisors preferentially function for cutting the molars grind the foodThe surface area of the molar process is slightly sclerotized During feeding thelong sharp spines of the maxillipeds and the palps of the rst maxillae point to themouth area ( g 7) which helps in handling the food thus facilitating the work ofthe mandibles


Fig 8 The labrum of Cyphocaris challengeri Stebbing 1888

The mandible of Cyphocaris challengeri

The mandibles are slender and elongated with a strong integument they insertlaterally on the head and meet frontally under the narrow apex of the labrum Thelabrum is small attened and drop-shaped with a frontal apex ( g 8) It onlycovers the proximal parts of the incisors The labium is triangular and bilobateThe mandibles t between the labrum and the labium with the mouth locatedabove the mandibles ( g 9) The incisors are toothless axe-like and sclerotizedThe lacinia mobilis is columnar narrow toothed and present only on the leftmandible ( g 10) When the mandibles close the left mandible embraces the right


Fig 9 Schematic representation of Cyphocaris challengeri Stebbing 1888 left mandible showingits position with respect to other mouthparts

one between the right incisor and the lacinia mobilis The seta row between theincisor and the molar is composed of 6 long strong setae that bear small serrationsThe molar is cuboid compact highly sclerotized and fringed with bundles of nesetae along its internal margin Its triturative surface consists of a regular patternof ridges across the molar The mandibular palps are strong oriented frontally atboth sides of the labrum and operate both frontally and on the basal area of theantennae

Function of the mandible of Cyphocaris challengeri

The incisors are frontally oriented and their toothless axe-like cutting edgesindicate they work as a pair of sharp scalpels The mandibles t between thelabrum and the labium and meet in a narrow region under the apex of the shield-shaped labrum ( gs 8-9) This arrangement suggests limited opening since thelabrum shape and size determine the bite gap (Manton 1977) During biting theright incisor may glide between the left incisor and the lacinia mobilis followinga curved path that their wedge shape dictates The distal indentation on the leftincisor may be clasped onto the hook ending of the right incisor The seta rowadjacent to the incisor is composed of long and strong setae that seem capableof holding large pieces of food and directing them towards the molar The spacebetween the incisor and the molar is large and suggests a capability for handling


Fig 10 Scanning electron microscope image of Cyphocaris challengeri Stebbing 1888 leftmandible

relatively large pieces of food When the mandibles close the molars cometogether presumably crushing the food between them While feeding the palpsfrom the mandible and the maxillipeds meet on the mid-line helping to hold thefood for biting or to prevent it from escaping The long spines and the tooth-likespines of the proximal endite all oriented medially help to hold the food and tosupport and guide it towards the mandibles

Morphometrics of the mandible of Parathemisto paci ca

The changes in dimension for the incisor and molar during growth are shownin gs 11-14 The change in molar dimensions related to the body growth ofParathemisto paci ca is allometric in nature The molar length shows a logarithmicrelationship with body size The molar length rapidly increases with body size from2 to 7 mm and then remains almost constant for the remaining sizes ( g 11) Incomparison molar height exhibits a slight increase in the 2-7 mm size interval( g 12) and beyond this size its height increases more acutely In fact the molarprocess changed shape throughout growth in small specimens it is round and shortwith a wide surface area that changes into a tall columnar molar process with aslender and lanceolate surface area in large specimens The number of teeth on the


Fig 11 Morphometric relation between body size and mandible characteristics of Parathemistopacica Stebbing 1888 Molar length and body size ( lled circles continuous line) follow therelation Y 4568 LNY 4088 (r2 084 n 38) Incisor length and body size (open

circles dotted line) follow the relation Y 1026 e0214X (r2 071 n 38)

Fig 12 Morphometric relation between body size and molar height of Parathemisto pacicaStebbing 1888 The trend line follows the relation Y 7046 1829X 187X2 (r2 081

n 38)

incisor increases from 7 to 12 in the 2-5 mm size range organisms to 12 to 14 ingt5-13 mm size range organisms in organisms of 13 mm up to a maximum sizeof 16 mm the incisor only acquires one more tooth while the length of the incisorincreases exponentially ( g 13) Finally the height of the incisor and the body sizefollow a quadratic relationship suggesting allometry in the morphological changeof the incisor during growth ( g 14)

Morphometrics of the mandible of Cyphocaris challengeri

The dimensions of the molar and incisor processes increase linearly with bodysize ( gs 15-17) and only differ in how rapidly those dimensions change withthe animalrsquos growth The height and the base of the incisor grow more slowlythan do molar height and incisor length This indicates that during growth the


Fig 13 Morphometric relation between body size and number of teeth in the incisor of Parathemistopacica Stebbing 1888 Trend line follows the relation Y 3637 LNX 5573 (r2 092

n 38)

Fig 14 Morphometric relation between body size and incisor height of Parathemisto pacicaStebbing 1888 Trend line follows the relation Y 0093X2 2047X 0066 (r2 090

n 38)

incisor widens while the molar process becomes shorter narrower and presumablysturdier These relationships indicate that the change in mandible shape during thegrowth of C challengeri is isometric

Stomach contents

Five-hundred-and-sixty-ve amphipods (307 Parathemisto paci ca and 258Cyphocaris challengeri) were dissected and their stomach contents were analysedIngested prey was identi ed in about 50 of the stomachs dissected 140 itemswere documented for Parathemisto paci ca and 116 for Cyphocaris challengeri


Fig 15 Morphometric relation between body size and molar dimensions of Cyphocaris challengeriStebbing 1888 Molar length and body size ( lled circles continuous line) follow the relationY 7852X 10068 (r2 095 n 32) Molar height and body size (open circles dotted

line) follow the relation Y 9943X 2045 (r2 096 n 32)

Fig 16 Morphometric relationbetween body size and incisor dimensions of Cyphocaris challengeriStebbing 1888 Incisor length and body size ( lled circles continuous line) follow the relationY 1583X 789 (r2 098 n 32) Incisor base width and body size (open circles dotted line)

follow the relation Y 703X 711 (r2 093 n = 32)

The most common groups identi ed in stomach contents were copepods cladocer-ans and ostracodes Both amphipod species were frequently found to prey uponeach other and even on their own species Larvae of barnacles bryozoans crabsand euphausiids were also present in the diet of both species although less fre-quently each accounting for less than 1 (and not shown in the percentage com-position in gs 16-17)


Fig 17 Morphometric relation between body size and incisor height of Cyphocaris challengeriStebbing 1888 Trend line follows the relation Y 4188X 0152 (r2 095 n 32)

Stomach contents of Parathemisto paci ca

The stomach contents of P paci ca contained small copepods amphipodscladocerans ostracodes crustacean larvae diatoms and euphausiids Copepodscomposed 52 of their diet followed by amphipods (33) including P paci caitself and C challengeri The results of the size frequency and nature of the preyfound in stomach contents suggest Parathemisto paci ca with body size from 2 to12 mm ( g 18A B) primarily consume copepods The size range in which theyingest ostracodes and the amphipod C challengeri was from 3 to 9 mm

The size range of the prey found in the stomach contents of P paci ca was 03to 3 mm ( g 18B) with a mean prey size of 096 mm and a standard deviationof 058 mm The size range of P paci ca studied was from about 2 to 12 mmThroughout its size range P paci ca ingested prey within the minimum prey sizeand progressively ate larger prey as its body size increased Large and completeprey items were more frequently found in the stomach contents of individualsmeasuring 6 to 9 mm

Stomach contents of Cyphocaris challengeri

Data suggested that C challengeri ingested small prey throughout the sizerange studied (of 2 to 16 mm) C challengeri ingested amphipods including theirown youngsters as well as P paci ca (41) copepods (33) cladocerans andostracodes ( g 19A) Bryozoa cyphonautes larvae and barnacle larvae were foundin the stomachs of C challengeri ranging from 8 to 14 mm and diatoms werefound in the stomachs of individuals ranging from 9 to 14 mm Fig 19B showsthat the size range of the prey found in dissected stomachs of C challengeri was045-25 mm with a mean size of 094 mm and a standard deviation of 039 mm


Fig 18 A Prey composition in the stomach contents of Parathemisto pacica Stebbing 1888B prey items identi ed at species or group level in 63 stomachs examined for Parathemisto pacicaStebbing 1888 The number of times the prey was found in stomach contents is given in parenthesesPrey size range was 03-30 mm mean value 096 mm and standard deviation 058 mm

Pteropod Limacina helicina Phipps 1774

As expected the largest prey size present in the stomach contents increased atlarger body sizes of C challengeri but what was mainly observed was an increasein the number of prey with growth

DISCUSSION

Mandible morphology

The morphology of the mandible of Parathemisto paci ca and Cyphocarischallengeri exhibits similar elements However a closer look at the particularmorphology of each species indicates functional differences in their action that


Fig 19 A Prey composition in the stomach contents of Cyphocaris challengeri Stebbing 1888B prey items identi ed at species or group level in 57 stomachs of Cyphocaris challengeri Thenumber of times the prey found in stomach contents is given in parentheses Prey size range was045-25 mm mean value 094 mm and standard deviation 039 mm Pteropod Limacina

helicina Phipps 1774

presumably could affect what they eat and thus their trophic ecology Literature onfunctional morphology of the mandible in amphipods relates a wide molar similarto that present in P paci ca to herbivorousmicrophagous habits (Watling 1993)while the stout crushing molar of the gammaridean C challengeri is related tocarnivorous habits (Sainte-Marie 1984) In both P paci ca and C challengeri themandible is elongate with the incisor at its front which is generally associated withthe ability to cut large pieces of food in carnivorous species (Watling 1993)

Toothed incisors as those found in P paci ca are present in hyperiids thatfeed on soft food (eg Lestrigonus schizogeneios Stebbing 1888 and Hyperiettastebbingi Bowman 1973) L schizogeneios is known to feed on marine snowand has also been found to burrow on the mesogloea of the medusa Aequorea


sp (Harbison et al 1977) which may indicate that it also feeds on gelatinousplankton L schizogeneios has a wide molar with blunt cusps (Bowman 1973)similar to those found in P paci ca The molar of H stebbingi is reduced comparedto that of P paci ca and has sharp cusps on the molar surface (Bowman 1973)This species feeds on egg masses and radiolarians (Harbison et al 1977) Bycontrast it may be inferred that the blunt lamelliform cusps found in the molar of Ppaci ca serve for crushing masses of soft food such as the organic matter found inmarine snow and perhaps also serve for breaking microzooplankton exoskeletonsthat may be present in marine snow or in particulate matter

The ability of the mandibles to cut large pieces of food the ample digestivechamber and the tendency of hyperiids to feed on soft tissue found in gelatinousplankton (Laval 1980) suggests this may be a food source for P paci ca Howeverthe protected nature of the foregut and evidence of raptorial habits in the relatedspecies P gaudichaudii (Gueacuterin 1825) (cf Sheader amp Evans 1975) and thepresence of a wide molar in P paci ca also suggest this species is capable offeeding on organisms with exoskeleton and therefore possesses some raptorialcapability

The non-linear morphometric relationships between elements of the mandibleof P paci ca indicate that the change in mandible shape during growth is allomet-ric This suggests that the mandible capability and feeding habits of P paci ca maychange during growth Young individuals have a wider molar than do adults indi-cating perhaps an acute microphagy early in life while the incisor of adults is widerand taller than that of small individuals which is indicative of carnivorous habits

The sharp toothless incisor of Cyphocaris challengeri is commonly found inspecies belonging to the family Lysianassidae and is considered an adaptation ofcarnivores for shearing-off large pieces of food (Steele amp Steele 1993 Watling1993) Lyssianasids with incisor-bearing mandibles but reduced or lacking molarprocesses have predominantly necrophagous habits and their stomachs containlarge pieces of soft food (Sainte-Marie 1984 Broyer amp Thurston 1987) Onthe other hand big-sized scavengers observed to possess a vestigial molar (egAnonyx sarsi Steel amp Brunel 1968 cf Sainte-Marie amp Lamarche 1985) mayexhibit some predatory activity However predation was limited to weak prey andonly observed in large individuals with high swimming capability

Strong palps and molars and sharp incisors on the mandibles of Cyphocarischallengeri are indicative of its predacious nature Such mandible features enablethem to access food from exoskeleton-protected small planktonic invertebratesIn contrast the comparatively weaker mandibular palps and toothed comb-likeincisors in Parathemisto paci ca seem indicative of a lesser predacious capability

The morphometric relationships between elements of the mandible of C chal-lengeri are linear indicating that the change in mandible shape during growth


is isometric This suggests that as C challengeri grows there is an increase inmandible capabilities for crushing and cutting This would allow them to feed onbigger food particles It also suggests that C challengeri is a carnivore throughoutits life

Stomach contents

Considering the mandibular elements observed in Parathemisto paci ca it wasanticipated that its diet might consist of detritus small invertebrates and soft tissuefrom coelenterates or perhaps sh larvae The mandibular structure of C challen-geri suggested the type of food would include hard-shelled crustaceans and soft sh larvae as well Stomachs of both species contained a varied assortment of smallcrustaceans including their own species and each otherrsquos young Diatoms weremore abundant in P paci ca stomach contents perhaps indirectly from high con-sumption of copepods which feed on diatoms or directly from the microphagouscapability its mandible morphology indicates That these two species have a some-what overlapping diet may relate to the mandible morphology indicating carnivo-rous feeding in both species

Stomach contents indicated that both Parathemisto paci ca and Cyphocarischallengeri most frequently prey on copepods amphipods cladocerans andostracodes The prey was similar in size for both amphipods with P paci caconsuming prey over a somewhat wider size range There was no evidence of achange of prey type consumed over the size range analysed but the size of thesame prey type andor the number of prey did increase The amphipods appearedto select female copepods suggesting females as a preferred prey type perhapsbecause females can have a higher nutritious value when bearing eggs or simplybecause female copepods are far more numerous than males The difference in dietbetween the two species was that amphipods were more abundant in stomachs ofC challengeri and copepods were more numerous in the stomachs of P paci caCrustacean larvae were more abundant in C challengeri than in P paci ca whileeuphausiids were found only in the stomach of P paci ca

What is missing is prey that may have been eaten but did not show up inthe analyses The type of prey most likely to be missing in the stomachs wouldinclude jelly-like food (eg coelenterates) or food that is rapidly digested (egpartially decomposed food) If this is the case for P paci ca andor C challengerithen the stomach contents analysis is providing a diet composition biased towardsorganisms with hard to digest or indigestible structures (eg crustaceans) Theanalysis of zooplankton diets using eld samples can be biased towards thezooplankton species caught in the sample Although the possibility of feedingduring con nement could occur for some zooplankters Sheader amp Evans (1975)


observed that P gaudichaudii specimens had to be exposed to prey for 3-5 daysto accept it as a food source Their results from both laboratory prey selectionexperiments and gut content analysis of eld samples also indicated that a preyspecies was more likely to become their food if it had previously formed part ofthe diet of Parathemisto This suggests that the stomach contents of Parathemistoare close to its true diet

Finally predominance of small organisms particularly copepods (07 to 2 mm)in the diet of P paci ca and C challengeri indicate amphipods may serve as atrophic link between small mesozooplankton and bigger zooplankton consumersIn the Strait of Georgia juvenile salmon and herring have been observed to feedin the Fraser River plume and estuarine plume areas (St John et al 1992) Inparticular sockeye salmon have been observed feeding on P paci ca both duringjuvenile and adult stages (cf Beacham 1986) Also large juvenile pink salmonwere observed to consume P paci ca (cf Beacham 1986) Considering that typeand quantity of prey may limit the survival of young sh (Lasker 1975 Arthur1976) amphipods may bene t the sh species that prey on them by concentratingfood energy and biomass from small zooplankton

In summary the feeding habits inferred from the shape and functional mor-phology of the mandible were reasonably close for both species as the stomachcontents indicated Similarities in the diet composition are thought to derive froma shared carnivorous capacity in the amphipod species studied although the shapeand functional morphology of the mandible indicated different feeding strategyfor each species Exclusive carnivory and pelagic habits suggest C challengeri isan active predator whereas microphagycarnivory suggests P paci ca is a pas-sive predator This may also explain C challengeri preying more intensively onP paci ca than P paci ca on C challengeri

ACKNOWLEDGEMENTS

Dr Alan G Lewis Dr Geoffrey Scudder Dr Paul Harrison and Dr TaniaZenteno-Savin provided timely help and insightful advice during the review of themanuscript Dr Elaine Humprey (UBC Electron Microscope Facility) providedsupport on the SEM imaging work This study was developed using zooplanktonsamples and data obtained for Dr Paul Harrisonrsquos project ldquoPlankton Productionand Nutrient Dynamics in the Fraser River Plumerdquo Editorrsquos notes and commentsto a previous version of this work are deeply appreciated


REFERENCES

ARTHUR D K 1976 Food and feeding of larvae of three shes occurring in the CaliforniaCurrentSardinops sagax Engraulis mordax and Thrachurus symmetricus Fish Bull US 74 517-528

BARNARD J L 1958 Index to the families genera and species of the gammaridean Amphipoda(Crustacea) Occas Pap Allan Hancock Foundation 19 1-145

BEACHAM T D 1986 Type quantity and size of food of paci c salmon (Oncorhynchus) in theStrait of Juan de Fuca British Columbia Fish Bull US 84 77-89

BIRTWELL I K M WOOD amp D K GORDON 1984 Fish diets and benthic organisms in theestuary of the Somass River Port Alberni British Columbia Canadian Manuscr Rep Fishaquat Sci 1799 1-49

BODEN B B M W JOHNSON amp E BRINTON 1955 The Euphausiacea (Crustacea) of the northPaci c Bulletin of the Scripps Institution of Oceanography 6 287-400

BOUSFIELD E L 1973 Shallow-water gammaridean Amphipoda of New England 1-312(Cornell University Press Ithaca New York)

mdash mdash 1987 Amphipod parasites of shes of Canada Canadian Bull Fish aquat Sci 217 1-37mdash mdash 1995 A contribution to the natural classi cation of Lower and Middle Cambrian arthropods

food gathering and feeding mechanisms Amphipaci ca Journal of Systematic Biology 2 3-34

BOWMAN T 1960 The pelagic amphipod genus Parathemisto (Hyperiidea Hyperiidae) in thenorth Paci c and adjacent Arctic Ocean Proceedings of the United States National Museum112 (3439) 243-392

mdash mdash 1973 Pelagic amphipods of the genus Hyperia and closely related genera (HyperiideaHyperiidae) Smithsonian Contributions to Zoology 136 1-76

BOWMAN T E amp H E GRUNER 1973 The families and the genera of Hyperiidea (CrustaceaAmphipoda) Smithsonian Contributions to Zoology 146 1-64

BRODEUR R D 1990 A synthesis of the food habits and feeding ecology of salmonids inmarine waters of the north Paci c 1-38 (INPFC Doc FRI-UW-9016 Fish Res Inst UnivWashington Seattle)

BROYER C amp M H THURSTON 1987 New Atlantic material and redescription of the type ofspecimens of the giant abyssal amphipod Alicella gigantea Chevreux (Crustacea) ZoologicaScripta 16 335-350

CLIFFORD P J P J HARRISON M A ST JOHN K YIN M A WAITE amp L J ALBRIGHT1991 (cf a) Plankton production and nutrient dynamics in the Fraser River plume 1989Manuscr Rep Univ British Columbia 54 1-225

CLIFFORD P J P J HARRISON K YIN M A ST JOHN amp R GOLDBLATT 1991 (cf b)Plankton production and nutrient dynamics in the Fraser River plume 1990 Manuscr RepUniv British Columbia 58 1-265

CLIFFORD P J P J HARRISON K YIN M A ST JOHN M A WAITE amp L J ALBRIGHT1990 Plankton production and nutrient dynamics in the Fraser River plume 1988 ManuscrRep Univ British Columbia 53 1-142

CLIFFORD P J K YIN P J HARRISON M A ST JOHN R GOLDBLATT amp D VARELA1992 Plankton production and nutrient dynamics in the Fraser River plume 1990 ManuscrRep Univ British Columbia 59 1-415

COLEMAN CH O 1991a Redescription of Anchiphimedia dorsalis (Crustacea AmphipodaIphimediidae) from the Antarctic and functional morphology of mouthparts ZoologicaScripta 20 367-374

mdash mdash 1991b Comparative fore-gut morphology of Antarctic Amphipoda (Crustacea) adapted todifferent food sources Hydrobiologia 223 1-9


HARBISON G R D C BIGGS amp L P MADIN 1977 The association of Amphipoda Hyperiideawith gelatinous zooplankton II Associations with Cnidaria Ctenophora and Radiolaria DeepSea Research 24 465-488

HARRISON P J P J CLIFFORD W P COCHLAN M A ST JOHN P A THOMPSON M JSIBBALD amp L J ALBRIGHT 1991 Nutrient and phytoplankton dynamics in the Fraser Riverplume Strait of Georgia British Columbia Mar Ecol Progr Ser 70 291-304

LASKER R 1975 Field criteria for the survival of anchovy larvae the relation between inshorechlorophyll maximum layers and successful rst feeding Fish Bull US 73 847-855

LAVAL P 1980 Hyperiid amphipods as crustaceanparasitoidsassociatedwith gelatinousplanktonOceanogr mar Biol ann Rev 18 11-56

MANTON S M 1977 The Arthropoda habits functional morphology and evolution 1-527(Clarendon Press Oxford)

MOORE P G amp P S RAINBOW 1984 Ferritin crystals in the gut caeca of Stegocephaloideschristianensis Boeck and other Stegocephalidae (Amphipoda Gammaridea) a functionalinterpretationPhil Trans R Soc London (B) 306 219-245

mdash mdash amp mdash mdash 1989 Feeding biology of the mesopelagic gammaridean amphipod Parandaniaboecki (Stebbing 1888) (Crustacea Amphipoda Stegocephalidae) from the Atlantic OceanOphelia 3 1-19

NAIR K K C P G JACOB amp S KUMARAN 1973 Distribution and abundance of planktonicamphipods in the Indian Ocean In The biology of the Indian Ocean Ecological Stud 3349-356 (Chapman amp Hall and Springer-Verlag London and Berlin)

NEMOTO T 1970 Feeding pattern of baleen whales in the ocean In J H STEELE (ed) Marinefood chains 241-254

PENNAK R W 1978 Fresh-water invertebrates of the United States 1-803 (John Wiley NewYork)

REILLY S M amp P C WAINWRIGHT 1994 Ecological morphology and the power of integrationIn P C WAINWRIGHT amp S M REILLY (eds) Ecological morphology Integrative organis-mal biology 339-354 (The University of Chicago Press Chicago)

SAINTE-MARIE B 1984 Morphological adaptations for carrion feeding in four species of littoralor circalittoral lysianassid amphipods Canadian Journal of Zoology 62 1668-1674

SAINTE-MARIE B amp G LAMARCHE 1985 The diets of six species of carrion-feedinglyssianasidamphipods genus Anonyx and their relation with morphology and feeding behavior Sarsia 70119-126

SCHMITZ E H 1992 Amphipoda In F W HARRISON (ed) Microscopic anatomy of inverte-brates 10 Crustacea 443-528 (Wiley-Liss New York)

SHEADER M amp F EVANS 1975 Feeding and gut structure of Parathemisto gaudichaudi(Gueacuterin) (Amphipoda Hyperiidea) Journal of the Marine Biological Association of the UnitedKingdom 55 641-656

STEELE D H amp V J STEELE 1993 Biting mechanisms of the amphipod Anonyx (CrustaceaAmphipoda Lysianassoidea) Journal of Natural History London 27 851-860

ST JOHN M A J S MACDONALD P J HARRISON R J BEAMISH amp E CHOROMANSKI1992 The Fraser River plume some preliminary observations on the distribution of juvenilesalmon herring and their prey Fisheries Oceanography 1 (2) 153-162

WATLING L 1989 A classi cation system for crustacean setae based on the homology concept InB FELGENHAUER amp L WATLING (eds) Functional morphology of feeding and grooming inCrustacea Crustacean Issues 6 15-26 (Balkema Rotterdam)

mdash mdash 1993 Functional morphology of the amphipod mandible Journal of Natural History London27 837-849

First received 4 December 2002Final version accepted 19 August 2003


wird Zur Pruumlfung dieser Hypothese wurden Zooplanktonproben von drei Standorten der Georgia-Straszlige Britisch-Columbia untersucht aus der Fahne des Fraser Flusses der Muumlndungsfahne undder Georgia-Straszlige Untersucht wurden der Bau der Mandibel der Mageninhalt und die potentielleNahrung der Amphipoden Parathemisto pacica und Cyphocaris challengeri

Rasterelektronenmikroskopische Aufnahmen der Mandibel und morphometrischeAnalysen wur-den benutzt um auf Nahrungsgewohnheitenruumlckzuschlieszligen Die Mandibel von P pacica hat einebreite pars molaris die auf Mikrophagiehindeutet und eine Schneidekantedie eher eischfressendeGewohnheiten nahelegt C challengeri dagegen scheint mit seiner kraumlftigen pars molaris und schar-fen Schneidekante der Mandibel ein richtiger Fleischfresser zu sein Die Mageninhaltsuntersuchun-gen zeigten dass sowohl Parathemistopacica als auch Cyphocaris challengerihauptsaumlchlich Cope-poden Amphipoden Cladocerenund Ostracoden erbeutenBeide scheinen Copepoden-Weibchenzubevorzugen entweder wegen ihres houmlheren Naumlhrwerts wenn sie Eier tragen oder weil sie die Maumln-nchen an Zahl uumlbertreffen Der Unterschied in der Nahrung beider Arten bestand darin dass derMagen von C challengeri mehr Amphipoden und der von P pacica mehr Copepoden enthielt DieTatsache dass kleine Copepoden-Artenzur Nahrung von Amphipoden gehoumlren legt nahe dass dieseein wichtiges Bindeglied zwischen dem Nanoplankton von dem sich die Copepoden ernaumlhren undFischen sind (zB Salmoniden und Clupeiden) die Amphipoden verzehren

INTRODUCTION

Amphipods are abundant in cold environments (Bowman amp Gruner 1973)particularly in highly productive estuarine areas (Nair et al 1973) as the Straitof Georgia British Columbia (St John et al 1992) They can be an important partof the diet of whales (Nemoto 1970) and sh (Birtwell et al 1984 St John et al1992) including salmon (Beacham 1986 Brodeur 1990) and keen zooplanktonpredators as well (Sheader amp Evans 1975) Knowledge of the feeding habits ofamphipods can provide a better understanding of the role they play in the trophicecology of the Strait of Georgia estuary

The study reported here was based on the hypothesis that because of environ-mental adaptations there is a strong relationship between morphology and ecolog-ical characteristics (Reilly amp Wainwright 1994) The morphology of the mandibleand of the rest of the feeding appendages is widely used for taxonomic classi -cation of amphipods (Barnard 1958) and the variation across species has provedquite useful in phylogenetic research (Watling 1993 Bous eld 1995) Yet only ahandful of studies has focused on the connection between morphology of oral ap-pendages and ecology (eg Sainte-Marie 1984 Moore amp Rainbow 1989 Cole-man 1991a b Steele amp Steele 1993)

The premise was that the morphology of the mandible and feeding habits areclosely related Testing this hypothesis involved investigating the mandible mor-phology and stomach contents of the amphipods Cyphocaris challengeri Stebbing1888 and Parathemisto paci ca Stebbing 1888 species abundant in plankton col-lections from the Strait of Georgia The study devoted particular attention to themandible morphology because among the mouthparts of amphipods the mandible



















RESULTS




























n 38)






n 38)


n 38)


Stomach contents



















DISCUSSION

Mandible morphology
















Stomach contents








ACKNOWLEDGEMENTS



REFERENCES



























































RESULTS




























n 38)






n 38)


n 38)


Stomach contents



















DISCUSSION

Mandible morphology
















Stomach contents








ACKNOWLEDGEMENTS



REFERENCES


































































n 38)






n 38)


n 38)


Stomach contents



















DISCUSSION

Mandible morphology
















Stomach contents








ACKNOWLEDGEMENTS



REFERENCES











































n 38)


n 38)


Stomach contents



















DISCUSSION

Mandible morphology
















Stomach contents








ACKNOWLEDGEMENTS



REFERENCES


























































DISCUSSION

Mandible morphology
















Stomach contents








ACKNOWLEDGEMENTS



REFERENCES























































Stomach contents








ACKNOWLEDGEMENTS



REFERENCES













































ACKNOWLEDGEMENTS



REFERENCES










































REFERENCES









































diet and functional morphology of the mandible of two ... and functional.pdf · morphology, the...

Documents